Phylogenomic Systematics of the Spotted Skunks (Carnivora, Mephitidae, Spilogale)
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bioRxiv preprint doi: https://doi.org/10.1101/2020.10.23.353045; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 Phylogenomic systematics of the spotted skunks (Carnivora, Mephitidae, Spilogale): 2 Additional species diversity and Pleistocene climate change as a major driver of 3 diversification 4 Molly M. McDonough*,†, Adam W. Ferguson*, Robert C. Dowler, Matthew E. Gompper, and 5 Jesús E. Maldonado 6 *-Equally contributing lead authors 7 †-Corresponding Author 8 Molly M. McDonough, Ph.D. 9 Chicago State University 10 Department of Biological Sciences 11 9501 S. King Drive, WSC 290 12 Chicago, IL 60628-1598 13 [email protected] 14 (773) 995-2443 15 16 17 Abstract 18 Four species of spotted skunks (Carnivora, Mephitidae, Spilogale) are currently recognized: 19 Spilogale angustifrons, S. gracilis, S. putorius, and S. pygmaea. Understanding species 20 boundaries within this group is critical for effective conservation given that regional populations 21 or subspecies (e.g., S. p. interrupta) have experienced significant population declines. Further, 22 there may be currently unrecognized diversity within this genus as some taxa (e.g., S. 23 angustifrons) and geographic regions (e.g., Central America) never have been assessed using 24 DNA sequence data. We analyzed species limits and diversification patterns in spotted skunks 25 using multilocus nuclear (ultraconserved elements) and mitochondrial (whole mitogenomes and 26 single gene analysis) data sets from broad geographic sampling representing all currently 27 recognized species and subspecies. We found a high degree of genetic divergence among 28 Spilogale that reflects seven distinct species and eight unique mitochondrial lineages. Initial bioRxiv preprint doi: https://doi.org/10.1101/2020.10.23.353045; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 29 divergence between S. pygmaea and all other Spilogale occurred in the Early Pliocene (~ 5.0 30 million years ago) which was followed by subsequent diversification of the remaining Spilogale 31 into an “eastern” and “western” lineage during the Early Pleistocene (~1.5 million years ago). 32 These two lineages experienced temporally coincident patterns of diversification at ~0.66 and 33 ~0.35 million years ago into two and ultimately three distinct evolutionary units, respectively. 34 Diversification was confined almost entirely within the Pleistocene during a timeframe 35 characterized by alternating glacial-interglacial cycles, with the origin of this diversity occurring 36 in northeastern Mexico and the southwestern United States of America. Mitochondrial-nuclear 37 discordance was recovered across three lineages in geographic regions consistent with secondary 38 contact, including a distinct mitochondrial lineage confined to the Sonoran Desert. Our results 39 have direct consequences for conservation of threatened populations, or species, as well as for 40 our understanding of the evolution of delayed implantation in this enigmatic group of small 41 carnivores. 42 Keywords: Ultra-conserved elements, Mitogenomes, Species tree, Pleistocene climate 43 change, Mexican Transition Zone, North America 44 45 1. Introduction 46 The taxonomy of well-known species is often taken for granted as being fully resolved, 47 especially for less speciose and disproportionately studied groups such as mammals (Foley et al., 48 2016). In light of this, biologists studying such taxa tend to focus on genetic diversity below the 49 species level, such as designation of Evolutionary Significant Units (Moritz, 1994) or genetically 50 distinct groups or populations (Coates et al., 2018). This is especially true for North American 51 carnivores, a well-studied group within which much work has been conducted on genetic bioRxiv preprint doi: https://doi.org/10.1101/2020.10.23.353045; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 52 distinctiveness at or below the species level (Akins et al., 2018; Balkenhol et al., 2020; Barton 53 and Wisely, 2012; Nigenda-Morales et al., 2019; Wultsch et al., 2016). Although such work has 54 highlighted taxonomic uncertainties, (e.g., Gopalakrishnan et al., 2018; Sinding et al., 2018), the 55 overall alpha taxonomy of this group often remains unchanged and as such is readily perceived 56 as more or less resolved. 57 For the many mammals threatened with extinction (Tilman et al., 2017), including 58 carnivores and ungulates, changes of the underlying taxonomy can have direct consequences in 59 terms of conservation efforts (Brownlow, 1996; Gippoliti et al., 2018; Thomson et al., 2018), 60 with species often more valued from a conservation standpoint than are subspecies or local 61 populations (Isaac et al., 2004; Mace, 2004). Examples where taxonomic uncertainty has the 62 ability to threaten conservation efforts can be found in several threatened North American small 63 carnivores including the pygmy raccoon Procyon pygmaeus and dwarf coati Nasua nelsoni 64 (McFadden et al., 2008), island fox Urocyon littoralis (Hofman et al., 2015), and San Joaquin kit 65 fox Vulpes macrotis mutica (Dragoo and Wayne, 2003). Although definitive boundaries for 66 species recognition of some of these taxa appear debatable, especially from a genetic standpoint, 67 biologists recognize the need to at minimum, treat these populations as distinct management 68 units (Cuaron et al., 2009; Robertson et al., 2014). In the USA, for instance, the Endangered 69 Species Act allows listing of species, subspecies, or Distinct Population Segments (DPSs) of 70 vertebrates for special protections (Waples et al., 2018). Yet despite of the availability of 71 multiple categories for protecting vertebrates as outlined in the ESA, assigning groups of animals 72 to a particular category can have direct consequences on their conservation status (Gippoliti and 73 Amori, 2007; Mace, 2004; O'Brien and Mayr, 1991) and can even influence taxonomic status or 74 recognition (i.e., so-called ‘political species’; Karl and Bowen, 1999). bioRxiv preprint doi: https://doi.org/10.1101/2020.10.23.353045; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 75 Accurate depictions of species diversity within a lineage also have consequences beyond 76 conservation, including the understanding of their biogeography (Kreft and Jetz 2010; Escalante 77 2016), ecology (Isaac et al., 2004), and evolution (Upham et al., 2019). Species represent the 78 fundamental unit in macroecology and inaccurate or out of date taxonomies can confound 79 hypothesis testing (Isaac et al., 2004). For mammalian carnivores, macroecological studies on 80 topics ranging from the relationship between geographic range size and body size (Diniz-Filho 81 and Tôrres, 2002) to the evolution of delayed implantation (Thom et al., 2004) have often 82 incorporated inaccurate information for one particular group of small carnivores: skunks. 83 Within the 12 currently recognized species of skunks in the family Mephitidae (Dragoo, 84 2009), molecular-based studies have mostly focused on unravelling their inter-generic 85 relationships (Dragoo et al., 1993) or focused specifically on the systematics of hog-nosed 86 skunks in the genus Conepatus (Dragoo et al., 2003; Schiaffini et al., 2013). However, to date, 87 the evolutionary history and phylogenetic relationships of the different species of the genus 88 Spilogale Gray 1865 in particular have been poorly studied. As a result, the genus has been 89 plagued by taxonomic uncertainty since it was first described (Table 1). These mephitids are 90 distributed north to south from British Columbia to Costa Rica and east to west from West 91 Virginia to California, and inhabit a wide array of biogeographic regions with complex 92 geological and climatic histories. The four currently-recognized species (S. angustifrons, S. 93 gracilis, S. putorius, S. pygmaea; Dragoo, 2009) inhabit the following North American 94 biogeographic areas that have been well-characterized for mammals: Californian-Rocky 95 Mountain subregion (Escalante et al., 2013), northwestern North America (Shafer et al., 2010), 96 the warm deserts (Riddle and Hafner, 2006), the Great Basin (Riddle et al., 2014), the Mexican bioRxiv preprint doi: https://doi.org/10.1101/2020.10.23.353045; this version posted October 25, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 97 Transition Zone (Morrone, 2010; Morrone, 2015), the Alleghanian subregion (Escalante et al., 98 2013), and Central America (Gutiérrez-García